Abstract
Cultivation of crops requires nutrient supplements which are costly and impact the environment. Furthermore, global demands for increased crop production call for sustainable solutions to increase yield and utilize resources such as nutrients more effectively. Some entomopathogenic fungi are able to promote plant growth, but studies over such effects have been conducted under optimal conditions where nutrients are abundantly available. We studied the effects of Beauveria bassiana (strain GHA) seed treatment on the growth of maize (Zea mays) at high and low nutrient conditions during 6 weeks in greenhouse. As expected, B. bassiana seed treatment increased plant growth, but only at high nutrient conditions. In contrast, the seed treatment did not benefit plant growth at low nutrient conditions where the fungus potentially constituted a sink and tended to reduce plant growth. The occurrence of endophytic B. bassiana in experimental plant tissues was evaluated by PCR after 6 weeks, but B. bassiana was not documented in any of the above-ground plant tissues indicating that the fungus-plant interaction was independent of endophytic establishment. Our results suggest that B. bassiana seed treatment could be used as a growth promoter of maize when nutrients are abundantly available, while the fungus does not provide any growth benefits when nutrients are scarce.
Similar content being viewed by others
References
Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrance D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818
Montanez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28
Pineda A, Zheng S-J, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514
Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92:fiw194. https://doi.org/10.1093/femsec/fiw194
Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology 2nd edn. Academic Press, Amsterdam, pp 171–220
Behie SW, Jones SJ, Bidochka MJ (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119
Barelli L, Moonjely S, Behie SW, Bidochka MJ (2016) Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Mol Biol 90:657–664
Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107
Lopez DC, Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53–60
Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45
Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577
Behie SW, Bidochka MJ (2014) Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Appl Environ Microbiol 80:1553–1560
Kabaluk JT, Ericsson JD (2007) Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agric J 99:1377–1381
Liao XG, O’Brien TR, Fang W, St, Leger RJ (2014) The plant beneficial effects of Metarhizium correlate with their association with roots. Appl Microbiol Biotechnol 98:7089–7096
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586
McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR (2017) Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl 62:1–17
Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hubner) (Lepidoptera, Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211
Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Technol 27:28–41
Parsa S, Ortiz V, Vega FE (2013) Establishing fungal entomopathogens as endophytes: towards endophytic biological control. J Vis Exp (74):50360
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Landa BB, Lopez-Diaz C, Jimenez-Fernandez D, Montes-Borrego M, Munoz-Ledesma FJ, Ortiz-Urquiza A, Quesada-Moraga E (2013) In-planta detection and monitorization of endophytic colonization by a Beauveria bassiana strain using a new-developed nested and quantitative PCR-based assay and confocal laser scanning microscopy. J Invertebr Pathol 114:128–138
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997
SAS (1991) SAS system for statistical graphics1st edn. SAS Institute Inc., Cary
Tukey JW (1977) Exploratory data analysis. Addison-Wesley, Reading
Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39
Megali L, Schlau B, Rasmann S (2015) Soil inoculation increases corn yield and insect attack. Agron Sustain Dev 35:1511–1519
Keyser CA, Thorup-Kristensen K, Meyling NV (2014) Metarhizium seed treatment mediates fungal dispersal via roots and induces infections in insects. Fungal Ecol 11:122–131
Behie SW, Moreira CC, Sementchoukova I, Barelli L, Zelisko PM, Bidochka MJ (2017) Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nat Commun 8:14245
Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113
Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127
Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot 98:379–387
Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97
Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric Ecosyst Environ 44:123–141
Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325
Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41
Russo ML, Pelizza SA, Cabello MN, Stenglein SA, Scorsetti AC (2015) Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales). Biocontrol Sci Technol 25:475–480
Biswas C, Dey P, Satpathy S, Satya P, Mahapatra BS (2013) Endophytic colonization of white jute (Corchorus capsularis) plants by different Beauveria bassiana strains for managing stem weevil (Apion corchori). Phytoparasitica 41:17–21
Powell WA, Klingeman WE, Ownley BH, Gwinn K (2009) Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). J Entomol Sci 44:391–396
Dara SK, Dara SR, Dara SS (2013) Endophytic colonization and pest management potential of Beauveria bassiana in strawberries. J Berry Res 3:203–211
Santyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR (2016) Plant growth promoting bacterial endophytes. Microbiol Res 183:92–99
Acknowledgements
We thank Maya Pedersen for assistance in the greenhouse and Professor Helle Sørensen for statistical advice.
Funding
ST was supported by a Marie Curie Intra European Fellowship (grant no. 331125), the Foundations’ Postdoc Pool, and Osk. Huttunen Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tall, S., Meyling, N.V. Probiotics for Plants? Growth Promotion by the Entomopathogenic Fungus Beauveria bassiana Depends on Nutrient Availability. Microb Ecol 76, 1002–1008 (2018). https://doi.org/10.1007/s00248-018-1180-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-018-1180-6